Advertisement

Burden of illness of follicular lymphoma and marginal zone lymphoma

  • Neerav Monga
  • Loretta Nastoupil
  • Jamie Garside
  • Joan Quigley
  • Moira Hudson
  • Peter O’Donovan
  • Lori Parisi
  • Christoph Tapprich
  • Catherine Thieblemont
Original Article

Abstract

Follicular lymphoma (FL) and marginal zone lymphoma (MZL) are two subtypes of indolent B cell non-Hodgkin lymphoma (NHL) that account for approximately 20% and 12% of all NHLs, respectively. FL and MZL are rare conditions with orphan disease designations. We conducted a comprehensive review of the burden of FL and MZL that encompasses the epidemiological, real world clinical, economic, and humanistic impact of these diseases globally. A targeted literature search identified 31 eligible studies for review. Epidemiological coverage was poor, with data obtained for studies from only seven countries. The incidences of both subtypes were low: age-standardized incidence rates of FL ranged from 2.1/100,000 in France to 4.3/100,000 in the USA, while for MZL it varied geographically from 0.5/100,000 in Australia to 2.6/100,000 in the UK. The cumulative total direct healthcare costs for FL were higher for patients with progressive disease compared to those without ($30,890 vs. $8704 at 12 months, respectively) and main driver of costs related to the use of chemotherapy. Five-year overall survival was improved in patients with FL compared with MZL (e.g., 76.5% vs 60.7% in one study that reported on both subtypes). Mortality rates were particularly lower in female patients with FL aged < 60 years. However, limited outcome data for MZL patients were identified. FL and MZL contribute significant burden on healthcare systems and on patients globally, with delays in progression potentially leading to cost savings. More rigorous characterization of these two NHL subtypes, new and more effective treatments, and standardization of reporting would lead to a more robust understanding of future data in this disease area.

Keywords

MZL FL Epidemiology Costs Economics QoL 

Notes

Acknowledgments

The authors would like to thank Iain Fotheringham (ICON Plc) and Natalie Nkwor (funded by ICON Plc) for medical writing support in the development of this manuscript.

Compliance with ethical standards

Conflicts of interest

Neerav Monga, Jamie Garside, Lori Parisi, and Christoph Tapprich are employees of Janssen.

Loretta Nastoupil and Catherine Thieblemont received research support/honoraria from Janssen.

Joan Quigley, Moira Hudson, and Peter O’Donovan are employees of ICON plc and have received funding from Janssen to conduct/support this research.

Supplementary material

277_2018_3501_MOESM1_ESM.docx (350 kb)
ESM 1 (DOCX 350 kb)

References

  1. 1.
    MacDonald D, Prica A, Assouline S, Christofides A, Lawrence T, Sehn LH (2016) Emerging therapies for the treatment of relapsed or refractory follicular lymphoma. Curr Oncol 23(6):407–417.  https://doi.org/10.3747/co.23.3405 CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    European Medicines Agency (2018) Public summary of opinion on orphan designation: venetoclax for the treatment of mantle cell lymphomaGoogle Scholar
  3. 3.
    Marcus R, Davies A, Ando K, Klapper W, Opat S, Owen C, Phillips E, Sangha R, Schlag R, Seymour JF, Townsend W, Trneny M, Wenger M, Fingerle-Rowson G, Rufibach K, Moore T, Herold M, Hiddemann W (2017) Obinutuzumab for the first-line treatment of follicular lymphoma. N Engl J Med 377(14):1331–1344.  https://doi.org/10.1056/NEJMoa1614598 CrossRefPubMedGoogle Scholar
  4. 4.
    Jacobsen CA, Freedman AS (2012) Early stage follicular lymphoma, current management and controversies. Curr Opin Oncol 24(5):475–479.  https://doi.org/10.1097/CCO.0b013e328356898b CrossRefGoogle Scholar
  5. 5.
    Ghielmini M, Vitolo U, Kimby E, Montoto S, Walewski J, Pfreundschuh M, Federico M, Hoskin P, McNamara C, Caligaris-Cappio F, Stilgenbauer S, Marcus R, Trneny M, Dreger P, Montserrat E, Dreyling M (2013) ESMO guidelines consensus conference on malignant lymphoma 2011 part 1: diffuse large B-cell lymphoma (DLBCL), follicular lymphoma (FL) and chronic lymphocytic leukemia (CLL). Ann Oncol 24(3):561–576.  https://doi.org/10.1093/annonc/mds517 CrossRefPubMedGoogle Scholar
  6. 6.
    Salles G, Seymour JF, Offner F, Lopez-Guillermo A, Belada D, Xerri L, Feugier P, Bouabdallah R, Catalano JV, Brice P, Caballero D, Haioun C, Pedersen LM, Delmer A, Simpson D, Leppa S, Soubeyran P, Hagenbeek A, Casasnovas O, Intragumtornchai T, Ferme C, da Silva MG, Sebban C, Lister A, Estell JA, Milone G, Sonet A, Mendila M, Coiffier B, Tilly H (2011) Rituximab maintenance for 2 years in patients with high tumour burden follicular lymphoma responding to rituximab plus chemotherapy (PRIMA): a phase 3, randomised controlled trial. Lancet 377(9759):42–51.  https://doi.org/10.1016/S0140-6736(10)62175-7 CrossRefPubMedGoogle Scholar
  7. 7.
    (NCCN) NCCN (2018) NCCN clinical practice guidelines in oncology. B-Cell Lymphomas Version 2:2018Google Scholar
  8. 8.
    Dreyling M, Thieblemont C, Gallamini A, Arcaini L, Campo E, Hermine O, Kluin-Nelemans JC, Ladetto M, Le Gouill S, Iannitto E, Pileri S, Rodriguez J, Schmitz N, Wotherspoon A, Zinzani P, Zucca E (2013) ESMO consensus conferences: guidelines on malignant lymphoma. Part 2: marginal zone lymphoma, mantle cell lymphoma, peripheral T-cell lymphoma. Ann Oncol 24(4):857–877.  https://doi.org/10.1093/annonc/mds643 CrossRefPubMedGoogle Scholar
  9. 9.
    Hutton B, Salanti G, Caldwell DM, Chaimani A, Schmid CH, Cameron C, Ioannidis JP, Straus S, Thorlund K, Jansen JP, Mulrow C, Catala-Lopez F, Gotzsche PC, Dickersin K, Boutron I, Altman DG, Moher D (2015) The PRISMA extension statement for reporting of systematic reviews incorporating network meta-analyses of health care interventions: checklist and explanations. Ann Intern Med 162(11):777–784.  https://doi.org/10.7326/m14-2385 CrossRefPubMedGoogle Scholar
  10. 10.
    Chihara D, Ito H, Matsuda T, Shibata A, Katsumi A, Nakamura S, Tomotaka S, Morton LM, Weisenburger DD, Matsuo K (2014) Differences in incidence and trends of haematological malignancies in Japan and the United States. Br J Haematol 164(4):536–545.  https://doi.org/10.1111/bjh.12659 CrossRefPubMedGoogle Scholar
  11. 11.
    Chouhan J, Batra S, Gupta R, Guha S (2016) Gastrointestinal follicular lymphoma: using primary site as a predictor of survival. Cancer Medicine 5(10):2669–2677.  https://doi.org/10.1002/cam4.763 CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Khalil MO, Morton LM, Devesa SS, Check DP, Curtis RE, Weisenburger DD, Dores GM (2014) Incidence of marginal zone lymphoma in the United States, 2001-2009 with a focus on primary anatomic site. Br J Haematol 165(1):67–77.  https://doi.org/10.1111/bjh.12730 CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Kuper-Hommel MJJ, Van De Schans SAM, Vreugdenhil G, Van Krieken JHJM, Coebergh JWW (2013) Trends in incidence, therapy and outcome of localized nodal and extranodal marginal zone lymphomas: declining incidence and inferior outcome for gastrointestinal sites. Leuk Lymphoma 54(9):1891–1897.  https://doi.org/10.3109/10428194.2013.764421 CrossRefPubMedGoogle Scholar
  14. 14.
    Le Guyader-Peyrou S, Belot A, Maynadie M, Binder-Foucard F, Remontet L, Troussard X, Bossard N, Monnereau A (2016) Cancer incidence in France over the 1980-2012 period: hematological malignancies. Revue d'Epidemiologie et de Sante Publique 64(2):103–112.  https://doi.org/10.1016/j.respe.2015.12.017 CrossRefPubMedGoogle Scholar
  15. 15.
    Liu L, Wang H, Chen Y, Rustveld L, Liu G, Du XL (2013) Splenic marginal zone lymphoma: a population-based study on the 20012008 incidence and survival in the United States. Leuk Lymphoma 54(7):1380–1386.  https://doi.org/10.3109/10428194.2012.743655 CrossRefPubMedGoogle Scholar
  16. 16.
    Luminari S, Cesaretti M, Marcheselli L, Rashid I, Madrigali S, Maiorana A, Federico M (2010) Decreasing incidence of gastric MALT lymphomas in the era of anti-helicobacter pylori interventions: results from a population-based study on extranodal marginal zone lymphomas. Ann Oncol 21(4):855–859.  https://doi.org/10.1093/annonc/mdp402 CrossRefPubMedGoogle Scholar
  17. 17.
    Olszewski AJ, Castillo JJ (2013) Survival of patients with marginal zone lymphoma: analysis of the surveillance, epidemiology, and end results database. Cancer 119(3):629–638.  https://doi.org/10.1002/cncr.27773 CrossRefPubMedGoogle Scholar
  18. 18.
    Smith A, Crouch S, Lax S, Li J, Painter D, Howell D, Patmore R, Jack A, Roman E (2015) Lymphoma incidence, survival and prevalence 2004-2014: sub-type analyses from the UK's Haematological Malignancy Research Network. Br J Cancer 112(9):1575–1584.  https://doi.org/10.1038/bjc.2015.94 CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Teras LR, DeSantis CE, Cerhan JR, Morton LM, Jemal A, Flowers CR (2016) 2016 US lymphoid malignancy statistics by World Health Organization subtypes. CA Cancer J Clin 66(6):443–459.  https://doi.org/10.3322/caac.21357 CrossRefGoogle Scholar
  20. 20.
    Van Leeuwen MT, Turner JJ, Joske DJ, Falster MO, Srasuebkul P, Meagher NS, Grulich AE, Giles GG, Vajdic CM (2014) Lymphoid neoplasm incidence by WHO subtype in Australia 1982-2006. Int J Cancer 135(9):2146–2156.  https://doi.org/10.1002/ijc.28849 CrossRefPubMedGoogle Scholar
  21. 21.
    Beveridge R, Satram-Hoang S, Sail K, Darragh J, Chen C, Forsyth M, Reyes C (2011) Economic impact of disease progression in follicular non-Hodgkin lymphoma. Leuk Lymphoma 52(11):2117–2123.  https://doi.org/10.3109/10428194.2011.592623 CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Conconi A, Lobetti-Bodoni C, Montoto S, Lopez-Guillermo A, Coutinho R, Matthews J, Franceschetti S, Bertoni F, Moccia A, Rancoita PMV, Gribben J, Cavalli F, Gaidano G, Lister TA, Montserrat E, Ghielmini M, Zucca E (2015) Life expectancy of young adults with follicular lymphoma. Ann Oncol 26(11):2317–2322.  https://doi.org/10.1093/annonc/mdv376 CrossRefPubMedGoogle Scholar
  23. 23.
    Gangatharan SA, Maganti M, Kuruvilla JG, Kukreti V, Tiedemann RE, Gospodarowicz MK, Hodgson DC, Sun A, Tsang RW, Pintilie M, Crump M (2015) Clinical characteristics and early treatment outcomes of follicular lymphoma in young adults. Br J Haematol 170(3):384–390.  https://doi.org/10.1111/bjh.13451 CrossRefPubMedGoogle Scholar
  24. 24.
    Hirayama Y, Ishitani K, Ota S, Kurosawa M, Kondo T, Takimoto R, Mori A, Sakai H, Torimoto Y, Yamamoto S, Sato K, Iwasaki H, Kohda K, Ishida T, Kakinoki Y, Fukuhara T, Kato J (2014) Long-term survey of survival time, histological transformation, and secondary malignancies in Japanese patients with advanced-stage follicular lymphoma in the rituximab era: Hokkaido Hematology Study Group. Int J Hematol 100(3):281–289.  https://doi.org/10.1007/s12185-014-1629-4 CrossRefPubMedGoogle Scholar
  25. 25.
    Nabhan C, Byrtek M, Rai A, Dawson K, Zhou X, Link BK, Friedberg JW, Zelenetz AD, Maurer MJ, Cerhan JR, Flowers CR (2015) Disease characteristics, treatment patterns, prognosis, outcomes and lymphoma-related mortality in elderly follicular lymphoma in the United States. Br J Haematol 170(1):85–95.  https://doi.org/10.1111/bjh.13399 CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Prochazka V, Papajik T, Janikova A, Belada D, Kozak T, Salek D, Sykorova A, Mocikova H, Campr V, Dlouha J, Langova K, Furst T, Trneny M (2016) Frontline intensive chemotherapy improves outcome in young, high-risk patients with follicular lymphoma: pair-matched analysis from the Czech Lymphoma Study Group Database. Leukemia & Lymphoma 1–13.  https://doi.org/10.1080/10428194.2016.1213834 CrossRefGoogle Scholar
  27. 27.
    Pulte D, Gondos A, Brenner H (2012) Expected long-term survival of older patients diagnosed with non-Hodgkin lymphoma in 2008-2012. Cancer Epidemiol 36(1):e19–e25.  https://doi.org/10.1016/j.canep.2011.08.006 CrossRefPubMedGoogle Scholar
  28. 28.
    Lenglet J, Traulle C, Mounier N, Benet C, Munoz-Bongrand N, Amorin S, Noguera ME, Traverse-Glehen A, Ffrench M, Baseggio L, Felman P, Callet-Bauchu E, Brice P, Berger F, Salles G, Briere J, Coiffier B, Thieblemont C (2014) Long-term follow-up analysis of 100 patients with splenic marginal zone lymphoma treated with splenectomy as first-line treatment. Leuk Lymphoma 55(8):1854–1860.  https://doi.org/10.3109/10428194.2013.861067 CrossRefPubMedGoogle Scholar
  29. 29.
    Danese MD, Reyes CM, Gleeson ML, Halperin M, Skettino SL, Mikhael J (2016) Estimating the population benefits and costs of rituximab therapy in the United States from 1998 to 2013 using real-world data. Med Care 54(4):343–349.  https://doi.org/10.1097/MLR.0000000000000486 CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Griffiths RI, Gleeson ML, Mikhael J, Danese MD (2015) Impact on medical cost, cumulative survival, and cost-effectiveness of adding rituximab to first-line chemotherapy for follicular lymphoma in elderly patients: an observational cohort study based on SEER-Medicare. Br J Haematol 170(3):384-390.  https://doi.org/10.1111/bjh.13451 CrossRefGoogle Scholar
  31. 31.
    Horsboel TA, Nielsen CV, Nielsen B, Jensen C, Andersen NT, de Thurah A (2013) Type of hematological malignancy is crucial for the return to work prognosis: a register-based cohort study. J Cancer Surviv 7(4):614–623.  https://doi.org/10.1007/s11764-013-0300-z CrossRefPubMedGoogle Scholar
  32. 32.
    Maurer MJ, Bachy E, Ghesquieres H, Ansell SM, Nowakowski GS, Thompson CA, Inwards DJ, Allmer C, Chassagne-Clement C, Nicolas-Virelizier E, Sebban C, Lebras L, Sarkozy C, Macon WR, Feldman AL, Syrbu SI, Traverse-Glehan A, Coiffier B, Slager SL, Weiner GJ, Witzig TE, Habermann TM, Salles G, Cerhan JR, Link BK (2016) Early event status informs subsequent outcome in newly diagnosed follicular lymphoma. Am J Hematol 91(11):1096–1101.  https://doi.org/10.1002/ajh.24492 CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Migdady Y, Salhab M, Dang NH, Markham MJ, Olszewski AJ (2016) Disparities in conditional net survival among non-Hodgkin lymphoma survivors: a population-based analysis. Leuk Lymphoma 57(3):676–684.  https://doi.org/10.3109/10428194.2015.1102246 CrossRefPubMedGoogle Scholar
  34. 34.
    Monnereau A, Troussard X, Belot A, Guizard AV, Woronoff AS, Bara S, Lapotre-Ledoux B, Iwaz J, Tretarre B, Maynadie M (2012) Unbiased estimates of long-term net survival of hematological malignancy patients detailed by major subtypes in France. Int J Cancer 132(10):2378–2387.  https://doi.org/10.1002/ijc.27889 CrossRefPubMedGoogle Scholar
  35. 35.
    Mounier M, Bossard N, Belot A, Remontet L, Iwaz J, Dandoit M, Girard-Boulanger S, Herry A, Woronoff AS, Casasnovas RO, Maynadie M, Giorgi R (2015) Trends in excess mortality in follicular lymphoma at a population level. Eur J Haematol 94(2):120–129.  https://doi.org/10.1111/ejh.12403 CrossRefPubMedGoogle Scholar
  36. 36.
    Nabhan C, Zhou X, Day BM, Dawson K, Zelenetz AD, Friedberg JW, Cerhan JR, Link BK, Flowers CR (2016) Disease, treatment, and outcome differences between men and women with follicular lymphoma in the United States. Am J Hematol 91(8):770–775.  https://doi.org/10.1002/ajh.24401 CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Nakamura S, Sugiyama T, Matsumoto T, Iijima K, Ono S, Tajika M, Tari A, Kitadai Y, Matsumoto H, Nagaya T, Kamoshida T, Watanabe N, Chiba T, Origasa H, Asaka M (2012) Long-term clinical outcome of gastric MALT lymphoma after eradication of Helicobacter pylori: a multicentre cohort follow-up study of 420 patients in Japan. Gut 61(4):507–513.  https://doi.org/10.1136/gutjnl-2011-300495 CrossRefPubMedGoogle Scholar
  38. 38.
    Olszewski AJ, Castillo JJ (2013) Comparative outcomes of oncologic therapy in gastric extranodal marginal zone (MALT) lymphoma: analysis of the SEER-Medicare database. Ann Oncol 24(5):1352–1359.  https://doi.org/10.1093/annonc/mds644 CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Olszewski AJ, Ali S (2014) Comparative outcomes of rituximab-based systemic therapy and splenectomy in splenic marginal zone lymphoma. Ann Hematol 93(3):449–458.  https://doi.org/10.1007/s00277-013-1900-4 CrossRefPubMedGoogle Scholar
  40. 40.
    Servitje O, Muniesa C, Benavente Y, Monsalvez V, Garcia-Muret MP, Gallardo F, Domingo-Domenech E, Lucas A, Climent F, Rodriguez-Peralto JL, Ortiz-Romero PL, Sandoval J, Pujol RM, Estrach MT (2013) Primary cutaneous marginal zone B-cell lymphoma: response to treatment and disease-free survival in a series of 137 patients. J Am Acad Dermatol 69(3):357–365.  https://doi.org/10.1016/j.jaad.2013.04.047 CrossRefPubMedGoogle Scholar
  41. 41.
    Stathis A, Chini C, Bertoni F, Proserpio I, Capella C, Mazzucchelli L, Pedrinis E, Cavalli F, Pinotti G, Zucca E (2009) Long-term outcome following Helicobacter pylori eradication in a retrospective study of 105 patients with localized gastric marginal zone B-cell lymphoma of MALT type. Ann Oncol 20(6):1086–1093.  https://doi.org/10.1093/annonc/mdn760 CrossRefPubMedGoogle Scholar
  42. 42.
    van de Schans SAM, van Steenbergen LN, Coebergh JWW, Janssen-Heijnen MLG, van Spronsen DJ (2014) Actual prognosis during follow-up of survivors of B-cell non-Hodgkin lymphoma in the Netherlands. Haematologica 99(2):339–345.  https://doi.org/10.3324/haematol.2012.081885 CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Pettengell R, Donatti C, Hoskin P, Poynton C, Kettle PJ, Hancock B, Johnson S, Dyer MJS, Rule S, Walker M, Wild D (2008) The impact of follicular lymphoma on health-related quality of life. Ann Oncol 19(3):570–576.  https://doi.org/10.1093/annonc/mdm543 CrossRefPubMedGoogle Scholar
  44. 44.
    Carter G, Liepa A, Zimmermann A, Morschhauser F (2008) Validation of the functional assessment of cancer therapy–lymphoma (FACT-LYM) in patients with relapsed/refractory mantle cell lymphoma. Paper presented at the American Society of HematologyGoogle Scholar
  45. 45.
    Oerlemans S, Issa DE, van den Broek EC, Nijziel MR, Coebergh JWW, Mols F, van de Poll-Franse LV (2014) Impact of therapy and disease-related symptoms on health-related quality of life in patients with follicular lymphoma: results of the population-based PHAROS-registry. Eur J Haematol 93(3):229–238.  https://doi.org/10.1111/ejh.12335 CrossRefPubMedGoogle Scholar
  46. 46.
    Tan D, Horning SJ, Hoppe RT, Levy R, Rosenberg SA, Sigal BM, Warnke RA, Natkunam Y, Han SS, Yuen A, Plevritis SK, Advani RH (2013) Improvements in observed and relative survival in follicular grade 1-2 lymphoma during 4 decades: the Stanford University experience. Blood 122(6):981–987.  https://doi.org/10.1182/blood-2013-03-491514 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Neerav Monga
    • 1
  • Loretta Nastoupil
    • 2
  • Jamie Garside
    • 3
  • Joan Quigley
    • 4
  • Moira Hudson
    • 4
  • Peter O’Donovan
    • 4
  • Lori Parisi
    • 5
  • Christoph Tapprich
    • 1
  • Catherine Thieblemont
    • 6
    • 7
    • 8
  1. 1.Janssen OncologyTorontoCanada
  2. 2.Department of Lymphoma/MyelomaThe University of MD Anderson Cancer CenterHoustonUSA
  3. 3.Janssen EMEA HEMARLondonUK
  4. 4.ICON Health Economics and EpidemiologyBostonUSA
  5. 5.Medical Affairs, JanssenRaritanUSA
  6. 6.APHP, Hemato-OncologyHôpital Saint-LouisParisFrance
  7. 7.Sorbonne Paris-CitéDiderot UniversityParisFrance
  8. 8.Descartes UniversityParisFrance

Personalised recommendations